Molecular phylogenetics and floral evolution in the sarracenioid clade (Actinidiaceae, Roridulaceae and Sarraceniaceae) of Ericales

Abstract

The sarracenioid families (Actinidiaceae, Roridulaceae, Sarraceniaceae) were rarely affiliated with other ericalean taxa in pre-molecular classifications and have seldom been considered closely related to each other. In molecular phylogenetic studies, the sarracenioids form a strongly supported clade and are sister to the ericoid clade (Clethraceae, Cyrillaceae, Ericaceae); the sarracenioids and ericoids together make up core Ericales. To date, no phylogenetic study has included all sarracenioid genera (Actinidia, Clematoclethra and Saurauia in Actinidiaceae; Roridula in Roridulaceae; Darlingtonia, Heliamphora and Sarracenia in Sarraceniaceae). In particular, the monophyly of Saurauia has not previously been tested using molecular characters. We shed light on the phylogenetic relationships within the sarracenioid clade and, based on ancestral state reconstructions, test floral characters previously suggested as potential synapomorphies for the sarracenioids and ericoids. Phylogenetic analysis was performed for the DNA regions ITS, rbcL, rpl32-trnL, trnK and trnL-F using RAxML, MrBayes and PAUP*. Our results support the monophyly of the sarracenioid clade as well as of all its families and non-monotypic genera. Two distinct geographical lineages are identified in Saurauia; the two lineages are characterised by differences in petal union (choripetaly versus sympetaly), style union (free versus partially united), gynoecium merism and base chromosome numbers. Our analyses identify the following floral characters as synapomorphic for core Ericales: adaxial anther attachment, anther inversion and a depression at the ovary-to-style transition. Proximally thick to massive petals, the presence of a nucellar hypostase in ovules and polystemony are synapomorphies of the sarracenioid clade. The presence of calcium oxalate raphides, mucilage cells, a secretory inner gynoecium surface and the absence of synlateral vasculature in the ovary are synapomorphies of the Actinidiaceae- Roridulaceae clade. A two-whorled androecium is a synapomorphy of the ericoid clade.

Full text

1209
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record
  
 || 
INTRODUCTION







      







 
aceae sister to 






Actinidia

Clematoclethra
  
Saurauia


  
Roridula


Darlingtonia

Heliamphora
   
Sarrace-
nia




Saurauia
have

Molecular phylogenetics and floral evolution in the sarracenioid clade
(Actinidiaceae, Roridulaceae and Sarraceniaceae) of Ericales
Stefan D. Löfstrand & Jürg Schönenberger
Depart ment of Botany and Biodiversity Research, University of Vienna, Rennweg 14, 1030 Vienna, Austria
 Stefan D. Löfstrand, stefan.loefstrand@univie.ac.at

DOI
  
Abstract
                                      

    


Actinidia

Clematoclethra
and
Saurauia
  
Roridula
   
Darlingtonia

Heliamphora
and
Sarracenia
 
Saurauia
 
  
  

rbcL

rpl32

trnL

trnK
and
trnL

F
 
     

Saurauia
  



  
   
 
Keywords
 

Supplementary Material




1210
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record

Actinidia

Clematoclethra
and
Saurauia
as outgroups

    




Sarracenia



Sau-
rauia

Actinidia

Clematoclethra

Saurauia

Saurauia


       
Darlingtonia

Sar-
racenia

Heliamphora


 
  
        



  
 
        


  








 
    



in
Darlingtonia





    


rbcL

rpl32

trnL

trnK

matK

trnK

trnL

trnF
   

is
Saurauia
 








 


MATERIALS AND METHODS
Sampling. —


Actinidia
 
species of
Clematoclethra scandens

Sau-
rauia

Roridula

Darlingtonia


Heliamphora

Sarracenia

Sarracenia purpurea






Camellia japonica



    
    

           
       
regions
rbcL

rpl32

trnL

rpl32-trnL
UAG
trnK

5t r n K - m a t K - 3 trnK

trnL-F

trnL
UAA
intron and
trnL
UAA 
trnF
GAA
DNA extraction, amplification and sequencing. —
   
        
  
 

    
             




    


 

       




  

 

 

1211
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record




           


Analyses. —


 



rpl32-trnL

trnK

trnL-F


rbcL



rbcL

rpl32-trnL

trnK

trnL-F
   
 
   
           
     
rbcL
datasets

     




  
   




 
   






Assessment of trees. —


    




     
  
 

         


ood    

Ancestral state reconstructions. —

  
 
    

 
  


   

      
  
  



Actinidia
arguta

A. chinensis

Clematoclethra scandens

Saurauia pittieri
 
S. subspinosa


Roridula gorgonias

Darlingtonia cali fornica
   
Heliamphora nutans

Sarracenia leucophylla
Raf
.
and
S. purpurea
 

Clethra alnifolia

Cyrilla racem-
iflora

Arbutus unedo

 
Cassiope mertensiana

   
Enkianthus campanulatus


Erica carnea
 
Harrimanella stelleriana

 
Monotropa hypopitys
        
Leucopogon amplexicaulis

Vaccinium vitis-idaea

Galax
urceolata

Styrax japonicus
 
Symplocos paniculata


Camellia japonica

Penta-
phylax euryoides

   

   

    
 

Monotropa hypopitys


   
M. hypopitys




   
as sup




 


        
    

1212
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record
Saurauia leprosa
Actinidia cylindrica
Actinidia melliana
Saurauia parviflora
Saurauia choriophylla
Camellia japonica
Actinidia valvata
Saurauia kegeiana
Actinidia zhejiangensis
Saurauia conferta
Actinidia fulvicoma
Actinidia polygama
Sarracenia purpurea subsp. purpurea
Actinidia rubricaulis
Saurauia aspera
Saurauia pedunculata
Sarracenia minor
Cyrilla racemiflora
Saurauia ferox
Actinidia persicina
Saurauia magnifica
Actinidia pilosula
Saurauia fasciculata
Harrimanella hypnoides
Actinidia latifolia
Saurauia scabrida
Arbutus canariensis
Enkianthus campanulatus
Actinidia kolomikta
Actinidia arguta
Saurauia pittieri
Actinidia chinensis
Clematoclethra scandens subsp. hemsley i
Sarracenia rubra
Sarracenia purpurea subsp. venosa
Sarracenia rosea
Sarracenia jonesii
Saurauia spectabilis
Saurauia subspinosa
Actinidia melanandra
Actinidia rudis
Saurauia malayana
Cassiope fastigiata
Saurauia ursina
Heliamphora pulchella
Heliamphora minor
Saurauia pentapetala
Heliamphora nutans
Sarracenia leucophylla
Clematoclethra scandens subsp. actinidioides
Saurauia roxbughii
Archeria comberi
Heliamphora ionasi
Saurauia polyneura
Sarrac enia flava
Saurauia bullosa
Saurauia macrotricha
Sarracenia oreophila
Actinidia macrosperma
Sarracenia psittacina
Actinidia hemsleyana
Actinidia rufa
Sarracenia alabamensis
Roridula dentata
Actinidia strigosa
Heliamphora heterodoxa
Saurauia chaparensis
Clethra arborea
Saurauia waldheimia
Saurauia tewensis
Darlingtonia californica
Actinidia chrysantha
Actinidia glaucophylla
Heliamphora neblinae
Chimaphila maculata
Heliamphora tatei
Saurauia novoguineensis
Saurauia napaulensis
Rhododendron ferrugineum
Actinidia indochinensis
Roridula gorgonias
Sarracenia alata
Actinidia sabiifolia
Actinidia callosa
Saurauia oreophila
Actinidia eriantha
Saurauia biserrata
Actinidia venosa
Saurauia montana
Saurauia yasicae
Actinidia styracifolia
Actinidiaceae
Roridulaceae
Sarraceniaceae
Neotropical
Saurauia clade
Asian-Oceanian
Saurauia clade
core Ericales
sarracenioid clade
ericoid clade
100 / 1 / 100
100 / 1 / 100
100 / 1 / 100
100 / 1 / 100
100 / 1 / 100
96 / 1 / 98
100 / 1 / 100
100 / 1 / 100
100 / 1 / 91
80 / 1 / 51
100 / 1 / 100
100 / 1 / 100
100 / 1 / 100
100 / 1 / 100
*
*
*
**
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
**
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
Gaultheria procumbens
Fig. 1.










1213
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record
       

  

RESU LT S
Molecular phylogenetic analyses. —

 
  
   
   
  

   
    


Saurauia


   




  
  
 

   
   
 

Heliamphora
and
Sarracenia

Actinidia
and
Clematoclethra
 


Clematoclethra
and
Dar-
lingtonia

Saurauia

              

Ancestral state reconstructions. —
  


    




   
   
  


          
  
    

  







   
Actinidia arguta
Actinidia chinensis
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula gorgonias
Darlingtonia californica
Heliamphora nutans
Sarracenia leucophylla
Sarracenia purpurea
Clethra alnifolia
Cyrilla racemif lora
Enkianthus campanulatus (Enkianthoideae)
Monotropa hypopitys (Monotropoideae)
Arbutus unedo (Arbutoideae)
Cassiope mertensiana (Cassiopoideae)
Erica carnea (Ericoideae)
Harrimanella stelleriana (Harrimanelloideae)
Leucopogon amplexicaulis (Styphelioideae)
Vaccinium vitis-idaea (Vaccinoideae)
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonica
Pentaphylax euryoides
Ericaceae
Sarraceniaceae
ericoid
clade
Actinidiaceae
Roridulaceae sarracenioid
clade
Clethraceae
Cyrillaceae
ingroup
outgroup
styracoid
clade
Diapensiaceae
Styracaceae
Symplocaceae
Theaceae
Pentaphylacaceae
Fig. 2.
 



1214
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record
Fig. 3.
 
A,
      
B,
   

C,

D,

E,

F,

B
Mucilage cells
in floral tissue
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia cali fornic a
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flor a
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium vitis-idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= present
= absent
= unknown /
equivocal
C
Proximal petal thickness
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia c alif ornica
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flora
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium v it is -idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= equal to or thicker
= than sepals
= thinner than sepals
= unknown /
equivocal
A
Calcium oxalate raphides
in floral tissue
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia c alif ornica
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flora
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium v it is -idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= present
= absent
= unknown /
equivocal
D
Secretory inner
gynoecium surface
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia cali fornic a
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flor a
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium vitis-idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= present
= absent
= unknown /
equivocal
E
Synlateral vasculature
in ovary
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia c alif ornica
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flora
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium v it is -idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= present
= absent
= unknown /
equivocal
F
Nucellar hypostase
in ovules
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia cali fornic a
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flor a
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium vitis-idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= present
= absent
= unknown /
equivocal

1215
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record
Fig. 4.
 
A,
   
B,
   
C,
orientation of anther attach

D,
         to 
  
 

E,

F,

A
Polystemony
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia c alif ornica
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flora
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium v it is -idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= present
= absent
B
Number of
androecium whorls
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia cali fornic a
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flor a
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic auli
s
Vaccinium vitis-idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= one
= two
= irregular
= unknown /
equivocal
C
Orientation of anther
attachment
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia c alif ornica
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flora
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium v it is -idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= abaxial
= adaxial
= proximal
D
Anther inversion
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia cali fornic a
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flor a
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic auli
s
Vaccinium vitis-idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= no inversion
= late type A
= late type B
= late type C
= early
E
Style union
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia c alif ornica
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flora
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic aulis
Vaccinium v it is -idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= partially free
= completely united
F
Depression at
ovary–style transition
Actinidia arguta
Actinidia c hinens is
Clematoclethra scandens
Saurauia pittieri
Saurauia subspinosa
Roridula g or gonias
Darlingtonia cali fornic a
Heliamphora nut an s
Sarracenia leucophylla
Sarracenia purpurea
Clethra alni foli a
Cyrilla racemi flor a
Enkianthus campanulatus
Monotropa hypopity s
Arbutus unedo
Cassiope mertensiana
Erica carnea
Harrimanella st elleriana
Leucopogon amplexic auli
s
Vaccinium vitis-idaea
Galax urceolata
Styrax japonicus
Symplocos paniculata
Camellia japonic a
Pentaphylax euryoides
= present
= absent
= unknown /
equivocal

1216
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record


 



 

     
 





    
 
 

 

Roridula


Clematoclethra


Clematoclethra
and
Roridula




the anthers of
Darlingtonia


Heliamphora- Sarracenia
     
      
  
Darlingtonia


Heliamphora- Sarracenia
 


Heliamphora


DISCUSSION
Molecular phylogenetic analyses. —
    
   
       



 

   
    

Clematoclethra
and
Darlingtonia


 

   

  

  
  
Actinidia
and
Clematoclethra


Saurauia
sister to the
Actinidia

Clematoclethra

       
   
Sau-
rauia

   

Saurauia


Saurauia



tionship of
Actinidia
and
Clematoclethra
 
        

Actinidia

Clematoclethra

Saurauia


Actinidia


Clematoclethra
and
Saurauia

Li
    

Actinidia



 
Actinidia


       


Actinidia
   

  
Actinidia

Actinidia

A.

Leiocarpae

A.

Strigosae
 and
A.

Vest itae

   


Within
Saurauia
      
    



Saurauia
and

  

Saurauia
focused









  

  


1217
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record


      




     





   
Saurauia



  

Heliamphora
and
Sarracenia
   
  
   
  
 

Sarracenia


Sarracenia
is addition
    

species in
Sarracenia
  
disputed
Sarracenia alabamensis

Sar-
racenia alata

Sarracenia jonesii

Sarracenia leucophylla
–
Sarracenia
rubra
  
   
Sarracenia
rosea
 
Sarracenia
purpurea

Heliamphora
a denser


  


Ancestral state reconstructions. —



  

   




   

     
for
Clematoclethra
and
Sarracenia

          

       
     

  

   
 

   
    
    

   
    
    


   
                        
   

 

   
Pole-
monium reptans
  


 

   

   
  







   
                        
           
      


          
Schwartzia brasiliensis
      

Rhododendron hirsutum
  
           
   



     


      


1218
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record
           
  
 


    
    


    

    



    
   


               



   

Roridula
are not nec
   
     

Saurauia


      
  
rounding the seeds of
Actinidia


     



         
  
 


Actinidia


   


Clematoclethra
and
Saurauia

 
  
Roridula
 
   

        
    
    


   
 
     




Clethra alnifolia

       
 
one investigated species of
Clethra

JS 552




description of
Clethra
 
      





  
  

& Bhatnagar
 
       
         
  

    
      

Roridula


Camellia
 


 

 



  
  
Actinidia chinensis

Camellia
 




 
Heliamphora



     Löfstrand & 

Darlingtonia
and
Sarracenia
of Sarraceniaceae both







1219
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record

           



Clematoclethra
and
Sarracenia

    
     


Cyrilla
 

Leucopogon



           
   






   

  
  

  

    



   
    
      
           

   
   










     

     

                       
do use this character to describe anther shape rather than the











          
 
  

  


   
    
case of
Darlingtonia




 
     

 





Heliamphora
and
Sarracenia

Darlingtonia
has anthers that invert at the onset of

          
 
    
  


Saurauia subspinosa
 

   


Cassiope

   

 




Actinidia

  



       

      

1220
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record
    
Heliamphora- Sarracenia

   




   


Clematocle-
thra

Heliamphora
and
Roridula


Actinidia

Saurauia

Darlingtonia
and
Sarracenia






          
          

   
   









Clematoclethra

Heliamphora

Roridula
 
    



  
Heliamphora

Sarracenia

in
Clethra

Arbutus
     
Actinidia

           



Roridula gorgonias


Darlingtonia californica

    
   
 

Actinidia



Actinidia


  
Darlingtonia
 


   

Similarities to floral mesofossils. —



Parasaurauia

 
Glandulocalyx
 

  
   

  
Glandulocalyx

 
Parasaurauia



   
  
Roridula
or
Saurauia

     
 

Parasaurauia

Glandulocalyx
and
Saurauia
  


SUMMARY AND CO NCLUSIONS

  

Actinidia

Clematoclethra

Heliamphora

Sarracenia
 

Saurauia


Saurauia
and supraspecific

Actinidia

Sarracenia


 







  
Heliamphora

Sarracenia


    
  
 
Roridula
  
Clematoclethra










1221
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
ACKNOWLEDGEMENTS

       
 
    
       
  

LITERATURE CITED
Alfaro, M.E. & Holder, M.T.             

Annual Rev. Ecol. Evol. Syst.


Alfaro, M.E., Zoller, S. & Lutzoni, F.  
 


Molec. Biol. Evol.

  
Anderberg, A.A. & Zhang, X.   
 
the genus
Purdiaea

Organisms Diversity Evol.


Anderberg, A.A., Rydin, C. & Källersjö, M.  
                     
 
Amer. J.
Bot.
 
Angiosperm Phylogeny Group      
                         

Bot. J. Linn. Soc.


Backer, C.A. & Bakhuizen van den Brink, R.C. 
Flora of Java


Gymnospermae, families 1–7; Angispermae, families 8–110.

Bhojwani, S.S. & Bhatnagar, S.P. 
The embryology of angio-
sperms

Boc, A., Boubacar Dial lo, A. & Makarenkov, V. 


Nucl. Acids Res

   
Brown, E.G. S.  
Saurauja subspinosa

Trans. & Proc. Bot. Soc. Edinburgh

    
Caris, P., Ronse De Craene, L.P. & Smets, E.F.  

Symplocos
     

Int. J. Pl. Sci.


Caris, P. 
Bloemontogenetische patronen in de Ericales sensu
lato

Chat, J., Jáuregui, B., Petit, R . & Nadot, S.        
 
Actinidia


Amer. J. Bot.
      

Conn, B.J. & Damas, K.Q. 
Saurauia
 

Telopea


Conran, J.G.   
The families and genera of vascular plants
 
Flowering
plants: Dicot yledons; Celastrales, Oxalidales, Rosales, Cor-
nales, Ericales.
 
Copeland, H.F.   
Madroño

Copeland, H.F. 

Madroño

Copeland, H.F.  
  
Phy-
tomorphology

Cronquist, A. 
An integrated system of classification of flowering
plants

Cui, Z., Huang, H. & Xingguo, X. 
in China

  
Cuong, N.M., Soejarto, D.D. & Li, J.  

Blumea
  

Dahlgren, R.      

Nordic J. Bot.


Darriba, E., Taboada, G.L., Daollo, R. & Posada, D. 
  
Nature,
Meth.
   
Dickison, W.C.   
 
Bot. J. Linn. Soc
 
   
Dressler, S. & Bayer, C.  
 
The families and genera of vascular plants

Flow-
ering plants: Dicot yledons; Celastrales, Oxalidales, Rosales,
Cornales, Ericales.
 
Dute, R.R., Folkerts, D.R., Watkins, J.E., Saxon, M.E. & Boyd. R.S.
 
Cyrilla racemi-
flora

S. E. Naturalist (Steuben)

 

Edgar, R.C. 

Nucleic Acid Res.

    
Ellison, A.M., Butler, E.D., Hicks, E. J., Naczi, R.F.C., Calie, P.J.,
Bell, C.D. & Davis, C.C.  

PLoS ONE


Endress, P.K.  
Diversity and evolutionary biology of tropical
flowers.

Erixon, P., Svennblad, B., Britton, T. & Oxelman, B. 
 

Syst. Biol.

   
Fritsch, P.W., Kelly, L.M., Wang, Y., Almeda, F. & Kriebel, R. 
    

Taxo n

Geuten, K., Smets, E., Schols, P., Yuan, Y.-M., Janssens, S., Küpfer,
P. & Pyck, N. 
                 

Molec. Phylogen. Evol.

    
Grant, V. 
Natural history of the phlox family.
   
Grubert, M. & Hambach, M. 

Collomia grandif lora

 
Beitr. Biol. Pf lanzen

Guindon, S. & Gascuel, O.         

Syst. Biol

 
   
He, Z.- C., Li, J.-Q., Cai, Q. & Wang, Q. 
Acti-
nidia
and
Clematoclethra

Bot. J. Linn. Soc.


Herrmann, P.M. & Palser, B.F.   
     

Amer. J. Bot



1222
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record
Hunter, G.E.  
Sau-
rauia

Ann. Missouri Bot. Gard.

   
Johri, B.M., Ambegaokar, K.B. & Srivastava, P.S. 
Compara-
tive embryology of angiosperms.
 
Kavaljian, L.G.    
Clethra alnifolia

C. acuminata
and
C. arborea. Bot. Gaz.


  
Keller, J.A., Herendeen, P.S. & Crane, P.R. 
 

Amer. J. Bot.


Konno, K., Inoue, T.A. & Nakamura, M. 

PLoS
ONE

Kron, K.A., Judd, W.S., Stevens, P.F., Crayn, D.M., Anderberg,
A.A., Gadek, P.A., Quinn, C. J. & Luteyn, J.L.  



Bot. Rev. (Lancaster)



Kubitzki, K. (ed.) 
The families and genera of vascular plants


Flowering plants: Dicotyledons; Celastrales, Oxalidales,
Rosales, Cornales, Ericales.
 
Lemke, D.E.   
 
Flora of North America north of
Mexico

Magnoliophyta: Paeoniaceae to Ericaceae


Li, J.-Q., Huang, H.-W. & Sang, T. 

Actinidia

Syst. Bot.

Li, J., Li, X. & Soejarto, D.D.    

Flora of China

Hippocas-
tanaceae through Theaceae
  
 
Li, X.-W. & Li, J.-Q. 

Actinidia

Ann. Bot. Fennici

 
Löfstrand, S.D. & Schönenberger, J.   
                 
 
Bot. J. Linn. Soc


Maddison, W.P. & Maddison, D.R.  
 

Magallón, S., Gómez-Acevedo, S., Sánchez-Reyes, L.L. & Hernán-
dez- Hernández, T. 

New Phytol.


Matthews, M.L. & Endress, P.K.  
        

Pl. Syst. Evol


Mauritzon, J. 

Bot. Not.


McPherson, S. & Schnell, D.E. 
Sarraceniaceae of North Amer-
ica

McPherson, S., Wistuba, A., Fleischmann, A. & Nerz, J. 
Sar-
raceniaceae of South America
 

Mellichamp, T.L.                 
            
Flora of North America north
of Mexico
 
Magnoliophyta: Paeoniaceae to Ericaceae

 
Min, T. & Bartholemew, B.   

Flora of China

Hippocastan aceae
through Theacea
    

Min, T. & Bartholemew, B.   

Flora of China

Hippocastanaceae
through Theaceae
   

Palser, B.F.                        

Bot. Gaz

  
Palser, B.F. 
  

Bot. Gaz

Palser, B.F.     
       

Phytomorphology

Palser, B.F.                       
  

Bot. Gaz.

   
Palser, B.F. 

Bot. Gaz.

  
Palser, B.F. & Murty, Y.S.  

Erica

Bull.
Torrey Bot. Club

Paterson, B.R.                        
Bot. Gaz.

Pirie, M.D. 
Taxo n

Qin, H. & Fritsch, P.     
 
Flora of China

Apiaceae through
Ericaceae


Rönblom, K. & Anderberg, A.A. 

Syst. Bot.

Ronquist, F., Huelsenbeck, J.P. & Teslenko, M. 
Draft MrBayes
version 3.2 manual: Tutorials and model summaries

 

Ronquist, F., Teslenko, M., Van den Mark, P., Ayres, D.L., Darling,
A., Höhna, S., Larget., B., Liu, L., Suchard., M.A . & Huelsen-
beck, J.P. 

Syst. Biol.
  
Ronse Decraene, L.P. & Smets, E.F.             

Bot. J. Linn.
Soc.

Schönenberger, J. 

Int. J. Pl. Sci.

 
Schönenberger, J., Anderberg, A.A. & Sytsma, K.J. 

Int.
J. Pl. Sci

Schönenberger, J., von Balthazar, M. & Sytsma, K.J.      


Philos. Trans., Ser. B.


Schönenberger, J., von Balthazar, M., Takahashi, M., Xiao, X.,
Crane, P.R. & Herendeen, P.S. 
Glandulocalyx upatoiensis

                            

Ann. Bot. (Oxford)
 

Simmons, M.P. & Norton, A.P.  

Molec. Phylog. Evol.

 
Soejarto, D.D.  
Saurauia. J. Arnold
Arbor


1223
Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
TAX ON
–
Version of Record
Soejarto, D.D. 
Saurauia
 
Rho-
dora

Soejarto, D.D.  
Revision of South American
Saurauia
(Actinidi-
aceae)

Soltis, D.E., Smith, S.A., Cellinese, N., Wurdack, K.J., Tank, D.C.,
Brockington, S.F., Refulio -Rodriguez, N.F., Walker, J.B.,
Moore, M.J., Carlsward, B.S., Bell, C.D., Latvis, M., Crawley,
S., Black, C., Diouf, D., Xi, Z., Rushworth, C.A., Gitzen danner,
M.A., Sytsma, K.J., Qui, Y.-L., Hilu, K.W., Davis, C.C.,
Sanderson, M.J., Beaman, R.S., Olmstead, R.G., Judd, W.S.,
Donoghue, M. J. & Soltis, P.S.  

Amer. J. Bot.
  

Stamatak is, A.  
 
Bioinformatics

  
Stephens, J.D., Rogers, W.J., Heyduk, K., Cruse-Sanders, J.M.,
Determann, R.O., Glenn, T.C. & Malmberg, R.L. 


Sarracenia

Molec. Phylogen.
Evol

Stewart, E.G.     
Bull.
Torrey Bot. Club

Sugiyama, M.  
 
Camellia japonica

J. Jap. Bot.


Sugiyama, M.   
Camellia japonica

J. Pl. Res.

Swofford, D.L. 
             

Tropicos   

Tsou, C.-H.                            
Amer. J. Bot.

Tucker, G.C. & Jones, S.C.             
            
Flora of North America
north of Mexico

Magnoliophyta: Paeoniaceae to Erica-
ceae

Van Royen, P. 
The alpine f lora of New Guinea

Taxonomic
part: Winteraceae to Polygonaceae.

Von Balthazar, M. & Schönenberger, J.   
      

Bot.
J. Linn. Soc.

Western, T.L. 

Seed Sci. Res.
  
Wu, Y. & Nootebom, H.P.  
 
Flora of China
 
Myrsinaceae
through Loganiaceae


Zhang, R.- J. & Schönenberger, J.  

Pl. Syst. Evol.

Appendix 1.
 
  
  
 rbcLrpl32-trnLtrnKtrnL-F
Actinidia arguta    Brownless 201 Actin-
idia callosaWang & al. 169 Actinidia chinensis  
Huang & al. 123              Actinidia chrysantha        
  Actinidia cylindricaActinidia eriantha
Actinidia fulvicoma             Actinidia glaucophylla       
 Actinidia hemsleyanaActinidia indochinensis
Actinidia kolomiktaBrownless 204
Actinidia latifolia       Actinidia macrosperma 
Actinidia melanandra Actinidia melliana        
 Actinidia persicina  Actinidia pilosula
Li & al. 12959          Actinidia polygama     
  Actinidia rubricaulis    Cuong 2051         
  Actinidia rudis   Cuong 2047 Actinidia rufa  
 Brownless 199  Actinidia sabiifolia
               Actinidia strigosa     Noshiro & al. 9240547     
      Actinidia styracifolia  Actinidia valvata 
         Actinidia venosaAldén & al. 1723            
Actinidia zhejiangensis   Arbutus canariensis      Archeria
comberi Camellia japonica Cassiope fastigiata
Crawford & al. 630Chimaphila maculata   
Clematoclethra scandens subsp. actinidioides     Clematoclethra scandens
subsp. hemsleyi Straley 5519         
  Clethra arborea  Cyrilla racemiflora           Darlingtonia californica    
 Löfstrand 4     Enkianthus campanulatus
    Gaultheria procumbens  Harrimanella hypnoides       
Heliamphora heterodoxa     Heliamphora ionasi 
Löfstrand 6             Heliamphora minor 
Löfstrand 7           Heli amphora neblinae           Heliamphora nutans 
 Löfstrand 8 Heliamphora pulchella 
Löfstrand 9            Heliamphora
tatei  Rhododendron ferrugineum  Roridula dentata 
 Roridula gorgonias    Löfstrand 3   

1224
TAX ON
–Löfstrand & Schönenberger • Sarracenioid systemat ics and f loral evolution
Version of Record
 Sarracenia alabamensis     Löfstrand 10            
      Sarracenia alata   Löfstrand 11  
     Sarracenia flava Löfstrand 12 
     Sarracenia jonesii  Sarracenia leucophylla Löf-
strand 13             Sarracenia minor Löfstrand 14 
                 Sarracenia oreophila      Löfstrand 15 
                 Sarracenia psittacina     Löfstrand 16 
 Sarracenia purpurea purpurea Löfstrand 17
          Sarracenia purpurea venosa 
Sarracenia rosea Löfstrand 18           
   Sarracenia rubra Löfstrand 5 
Saurauia aspera   Meyer 9964 Saurauia biserrata   
Croat 57648 Saurauia bullosa Rubio & al. 2234  
       Saurauia chaparensis Teran & al. 603          
     Saurauia choriophylla    Fonnegra & al. 5699  
   Saurauia conferta      Bau & al. 84182  Saurauia fasciculata
  Noshiro & al. 9755133            Saurauia ferox  Mantor 130145
Saurauia kegeliana Rodríguez & al. 747 
Saurauia leprosa Middleton & al. 3543 
Saurauia macrotricha Cuong 2040   Saurauia magnifica   
Harling & Anderson 12675 Saurauia malayana Julius & al.
57477    Saurauia montana  Schönenberger 908    
     Saurauia napaulensis   Gaoligong Shan Biodiversity Survey 23389  
 Saurauia novoguineensis Regalado & Sirikolo 786 Saurauia
oreophila Ávila & al. 3238 Saurauia parviflora Croat & Gas-
kin 80128 Saurauia pedunculata Cruz Paredes 147  
         Saurauia pentapetala Middleton & al. 3501        
     Saurauia pi ttieri Borg 17               Saurauia
polyneura Li & al. 8725 Saurauia roxburghii  
Newman & al. 2339 Saurauia scabrida Góme z Chagala
822 Saurauia spectabilis Fuentes & al. 10418 
    Saurauia subspinosa  Löfstrand 2         
   Saurauia tewensis Burley & al. 3345  Saurauia
ursina Gentry & al. 76191 Saurauia waldheimia Stevens & al.
29397   Saurauia yasicae   Aguilar 5581  

Appendix 1.
